Neural basis of emotional decision making in trait anxiety.

State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China, Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China, Department of Behavioral Science, University of Kentucky College of Medicine, Lexington, Kentucky 40536, School of Social and Political Science, University of Edinburgh, Edinburgh EH8 9LD, United Kingdom, Department of Psychiatry, New York University School of Medicine, New York, New York 10016, Department of Psychology, Queens College, City University of New York, New York 10075, Department of Psychiatry, Fishberg Department of Neuroscience, and Friedman Brain Institute, Mount Sinai School of Medicine, New York, New York 10029, and Institute of Affective and Social Neuroscience, Shenzhen University, Shenzhen 518060, China.

Abstract

Although trait anxiety has been associated with risk decision making, whether it is related to risk per se or to the feeling of the risk, as well as the underlying neurocognitive mechanisms, remains unclear. Using a decision-making task with a manipulation of frame (i.e., written description of options as a potential gain or loss) and functional magnetic resonance imaging, we investigated the neurocognitive relationship between trait anxiety and decision making. The classic framing effect was observed: participants chose the safe option when it was described as a potential gain, but they avoided the same option when it was described as a potential loss. Most importantly, trait anxiety was positively correlated with this behavioral bias. Trait anxiety was also positively correlated with amygdala-based "emotional" system activation and its coupling with the ventromedial prefrontal cortex (vmPFC) when decisions were consistent with the framing effect, but negatively correlated with the dorsal anterior cingulate cortex (dACC)-based "analytic" system activation and its connectivity to the vmPFC when decisions ran counter to the framing effect. Our findings suggest that trait anxiety is not associated with subjective risk preference but an evaluative bias of emotional information in decision making, underpinned by a hyperactive emotional system and a hypoactive analytic system in the brain.

Schematic of the decision-making task. For each trial, after a 2 s fixation, a certain amount of money (e.g., “you receive 100 points” in Chinese in the figure) is presented for 2 s. After that, a 4 s choice with a “sure” and a “gamble” option is displayed. The “sure” option states how much money will be retained from the initial amount (“keep 80 points”) in the gain frame and how much money will be lost from the initial amount (“lose 80 points”) in the loss frame. The “gamble” option states the probability of winning (in green) or losing (in red) the total amount of money for the trial, using a pie chart. The options were balanced across trials on the left and right side of the screen. A, Gain frame. B, Loss frame.

Brain activation of the framing effect and trait anxiety. A, Brain activation of the framing effect (i.e., the contrast of (Gsure + Lgamble) − (Ggamble + Lsure)). B, Correlations among activation of left amygdala ROI (−24, −4, −10), behavioral framing effect, and trait anxiety. C, Positive correlations between trait anxiety and neural activation for the framing effect based on whole-brain analysis. D, Deactivation of the framing effect (i.e., activation of the contrast of (Ggamble + Lsure) − (Gsure + Lgamble)). E, Correlations among activation of right dACC ROI (−40, 10, 2), behavioral framing effect, and trait anxiety. F, Negative correlations between trait anxiety and neural activation for the framing effect based on whole-brain analysis. For A and C, An amygdala mask from the AAL template was used; activation of other brain regions can be found in and .

Functional connectivity of vmPFC under the framing effect in trait anxiety. A, Activation of vmPFC was positively coupled with amygdala under the framing effect. B, The vmPFC–amygdala connectivity under framing effect was positive correlated with trait anxiety (p = 0.02; ROI analysis based on A). C, Positive correlations between vmPFC-based circuits and trait anxiety. D, Activation of vmPFC was negatively coupled with dACC under the framing effect. E, The vmPFC–dACC circuit under framing effect was not significant correlated with trait anxiety (p = 0.16; ROI analysis based on E). F, Negative correlations between vmPFC-based circuits and trait anxiety (whole-brain analysis). ForA and C, An amygdala mask from the AAL template was used; activation of other brain regions can be found in and .